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Green Leaf, Red Leaf, and Romaine Lettuce Breeding Lines with Resistance to Leafminer, Corky Root, and Downy Mildew

Author:
Beiquan Mou US Department of Agriculture, Agricultural Research Service, 1636 East Alisal Street, Salinas, CA 93905, USA

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Leafminers (Liriomyza spp.) are major insect pests of many important crops worldwide (Parrella 1987). The predominant leafminer species in the major lettuce (Lactuca sativa L.) production area of central costal California is Liriomyza langei (Scheffer et al. 2001). Leafminer adults are small, shiny, black flies with a bright yellow triangular spot on the upper thorax between the wings. Leafminer damage occurs when adult flies puncture leaves to feed on plant sap and when females lay eggs within the leaf tissue, leaving “stings” that appear as holes or bumps on the leaves. Larvae hatch from white, oval eggs and feed between upper and lower leaf surfaces, creating whitish, winding tunnels or mines (University of California 1992). Damage caused by adult stings and larval mining reduces photosynthetic capacity, renders lettuce leaves unmarketable, and provides entrances for disease organisms. Chemical control of leafminers usually lasts only a short period of time. Adult control with contact insecticides is especially problematic because flies can easily move around, and the treated field is subject to reinfestation from adjacent untreated crops and weeds (LeStrange et al. 1999). It has been well-documented that leafminers can develop a high degree of resistance to a broad range of insecticides (Keil and Parrella 1990; Mason et al. 1987; Parrella and Trumble 1989). Therefore, it is essential to develop alternative strategies for leafminer management, including the deployment of resistant varieties.

Corky root of lettuce has been found in major lettuce-producing areas of the world, including North America, Western Europe, Australia, and New Zealand. Roots of infected plants develop yellow to brown lesions that later become longitudinal corky ridges and restrict the absorption of water and nutrients. In severely infested fields in California and Florida, yield losses from reduced head size can reach up to 100%. The pathogen most commonly isolated from diseased roots is the bacterium Sphingomonas suberifaciens (Yabuuchi et al. 1999), formerly Rhizomonas suberifaciens, although several other bacterial species have been isolated (van Bruggen 1997). Cultural practices, such as crop rotation, cover cropping, reduced nitrogen fertilizers, drip irrigation, and improved soil drainage, may reduce corky root to a certain extent (Alvarez, et al. 1992; Subbarao et al. 1997; van Bruggen and Brown 1990; van Bruggen et al. 1990). The incidence of corky root can also be reduced by soil fumigation (O’Brien and van Bruggen 1990) and by using lettuce transplants instead of direct-seeding (van Bruggen and Rubatzky 1992); however, these practices may not be economically feasible (Patterson et al. 1986), and alternative strategies are needed. The use of cultivars resistant to S. suberifaciens has been an important management strategy for corky root. The resistance to corky root is conferred by a recessive allele (cor) at a single locus (Brown and Michelmore 1988), which has been deployed in most resistant lettuce cultivars.

Downy mildew, one of the most economically important diseases of cultivated lettuce worldwide, is caused by the biotrophic oomycete pathogen Bremia lactucae Regel. Lettuce, from young seedlings to mature plants, is susceptible to this pathogen. Infected plants develop yellow to pale green lesions that eventually become necrotic, leading to lower marketable yield and higher harvest-related costs because of the need to remove infected leaves. More than 30 major genes for downy mildew resistance have been identified in lettuce. The resistance based on single dominant major genes, however, has not been durable because new isolates of the pathogen have continued to evolve and render this race-specific resistance ineffective (Lebeda and Zinkernagel 2003). Quantitative or horizontal resistance has been shown to be determined polygenically and is considered more durable than single major genes. Quantitative resistance has been found in several lettuce cultivars that typically become infected with most races of the pathogen, but the lesions are small, with limited sporulation. Often this phenomenon is more evident in adult plants; therefore, it is designated as adult, partial, or field resistance (Simko et al. 2013). Two of the most resistant lettuce cultivars with such resistance to downy mildew are Iceberg and Grand Rapids, which were developed more than a century ago and are no longer used in lettuce production (Grube and Ochoa 2005). Resistance to downy mildew in these cultivars appears to be durable because they still appear resistant to the disease during our recent field trials, even though resistance was observed in Grand Rapids at least 50 years ago and in Iceberg more than 90 years ago.

The most economical means of insect and disease control is through the use of genetic resistance of plants. This is especially true for organic growers who cannot apply synthetic pesticides and must rely on a combination of natural resistance, organically certified pesticides, and cultural practices to combat insects and diseases. Repeated pesticide applications may allow pests/pathogens to develop resistance against the chemicals, resulting in the loss of efficacy. The use of resistant cultivars does reduce chemical usage, which benefits growers, consumers, and the environment. However, lettuce cultivars with a high level of resistance to leafminers are not currently available. We describe two green leaf, one red leaf, and two romaine lettuce breeding lines with combined resistance to leafminers, corky root, and/or downy mildew that are adapted to the major lettuce production areas of the central coast of California.

Origin

The red leaf breeding line USDA-07838 is the result of a cross between a green leaf lettuce PI 169513 as the male parent and a green romaine cultivar Lobjoits (Fig. 1). The green leaf breeding line USDA-09456 was derived from a cross between a crisphead cultivar Glacier that has cor alleles (Ryder and Waycott 1994) as the male parent and a red leaf cultivar Merlot that showed low leafminer sting density during previous screening experiments (Mou and Liu 2004). Another green leaf breeding line USDA-09512 originated from a cross between a red leaf cultivar Lolla Rossa that also had low leafminer sting densities in previous screening trials (Mou and Liu 2003, 2004) as the male parent and a crisphead cultivar Tiber (Ryder and Waycott 1998). USDA-14489 is a green romaine breeding line from a series of crosses: PI 509525 (L. saligna) was crossed as the male parent to the butterhead cultivar Margarita; an F3 progeny plant was selected as the male parent to hybridize to the green leaf cultivar Waldmann’s Green, and the resulting F1 was crossed as the female parent to the green romaine cultivar Clemente with the cor alleles. Another green romaine breeding line USDA-17536 was obtained from the hybridization between the male parent ‘Glacier’ and ‘Merlot’, and then with an F4 progeny plant selected as the male parent to cross to ‘Clemente’. The progeny plants from these crosses were selected in the field of the US Department of Agriculture (USDA), Agricultural Research Service (ARS) in Salinas, CA, for a lower density of leafminer stings and less severity of corky root and downy mildew, as well as horticultural traits in summer, when leafminers are abundant and diseases are prevalent. Single plant selections were made by using the pedigree method of breeding from the F2 to F6 generations, with the later generations evaluated during summer field trials at the USDA-ARS station in Salinas, CA.

Fig. 1.
Fig. 1.

Pedigrees of lettuce breeding lines USDA-07838, USDA-09456, USDA-09512, USDA-14489, and USDA-17536.

Citation: HortScience 58, 4; 10.21273/HORTSCI17069-22

Description

The red leaf breeding line USDA-07838 has a brown–red leaf color that becomes green toward the core (Fig. 2A). Its leaf margins have fine indents with mild undulations. The leaf surface is densely blistered. The outer leaves are broader than they are long. It has a flat bottom and moderately raised ribs. The leaves have a relatively soft and flexible texture as well as a bland and mild taste. The seed color is white.

Fig. 2.
Fig. 2.

Lettuce breeding lines in the field: (A, upper left): USDA-07838 (red leaf); (B, upper right): USDA-09456 (green leaf); (C, middle left): USDA-09512 (green leaf); (D, middle right): USDA-14489 (romaine); and (E, lower left): USDA-17536 (romaine).

Citation: HortScience 58, 4; 10.21273/HORTSCI17069-22

Both green leaf breeding lines USDA-09456 and USDA-09512 have glossy light-green leaves that extend close to the core on a partially trimmed head (Fig. 2B and 2C). The leaf margins of USDA-09456 have shallow, fine indents with mild undulations, whereas USDA-09512 has entire leaf margins that are slightly undulating. Their leaf surfaces are moderately crinkled or blistered. The outer leaves have approximately equal length and width. The bottom and ribs are flat, but the middle rib becomes more prominent toward the base. The texture is relatively soft and flexible. They have a mild and bland taste. The seed color is black.

The romaine breeding line USDA-14489 has dark-green leaves (Fig. 2D), whereas USDA-17536 has yellow-green leaves (Fig. 2E). The leaf margins of both lines are whole. They have a moderately blistered leaf surface. The outer leaves are longer than they are broad. The heads are initially open but later become closed. Bases of outer and interior leaves overlap well. USDA-14489 has flat ribs and USDA-17536 has slightly raised ribs. They have a crunchy texture and a bland taste. Both lines have a white seed color.

Insect and Disease Resistance

The breeding lines, along with commercial cultivars and resistance controls, were evaluated during trials at the Spence Farm of the ARS of the USDA, Salinas, CA, during multiple years. The experimental design was a randomized complete block with four replications. Each plot was 14 m long, with commercial spacing of 30 cm between plants and 35 cm between rows on a 1-m-wide double-row bed. Standard production practices were followed during each trial. At harvest maturity, five plants were randomly selected in each plot, and the number of leafminer stings was counted in a 20-cm2 leaf area with the highest sting density on each selected plant. The roots of five randomly selected mature plants from each plot were rated for corky root severity using a scale of 0 to 9 (0, no disease symptom; 9, plant died from disease) (Brown and Michelmore 1988). Five random plants in each plot were also rated for downy mildew disease by using a scale of 0 to 5 (0, no lesions; 5, large lesions covering nearly 100% of exposed leaf surface) (Grube and Ochoa 2005). Data collected were averaged for all plants in each plot, and an analysis of variance was conducted based on the plot means using the general linear model procedure of JMP (SAS Institute, Cary, NC). The genotype was considered a fixed effect, and replication was considered a random effect. For comparisons among genotypes, significant differences were calculated with a type I (α) error rate of P = 0.05.

The breeding lines had significantly lower leafminer sting density than resistant controls (‘Shining Star’, ‘Merlot’, and ‘Lolla Rossa’) and commercial cultivars in almost all the trials (Tables 13). The corky root ratings of the green leaf (USDA-09456 and USDA-09512) and romaine (USDA-14489 and USDA-17536) breeding lines were significantly lower than susceptible commercial cultivars but were generally not significantly different from the Clemente and Heart’s Delight cultivars with the cor gene (Tables 2 and 3). The two green leaf lines also had significantly lower downy mildew ratings than commercial cultivars, although the ratings were similar to those of the resistant controls Iceberg and Grand Rapids (Table 2). Other disease or insect reactions have not been tested.

Table 1.

Means of leafminer sting density (stings per cm2 leaf area), disease responses, and horticultural traits of the red leaf lettuce breeding line USDA-07838 and cultivars evaluated during field trials in Salinas, CA, from 2009 to 2021.

Table 1.
Table 2.

Means of leafminer sting density (stings per cm2 leaf area), disease responses, and horticultural traits of the green leaf lettuce breeding lines USDA-09456 and USDA-09512 and of cultivars evaluated during field trials in Salinas, CA, from 2010 to 2021.

Table 2.
Table 3.

Means of leafminer sting density (stings per cm2 leaf area), disease responses, and horticultural traits of the romaine lettuce breeding lines USDA-14489 and USDA-17536 and of cultivars evaluated in field trials in Salinas, CA, from 2017 to 2021.

Table 3.

Performance and Adaptation

During the field trials mentioned, five plants were randomly sampled from each plot to assess the horticultural traits. The height of the romaine lettuce plants was measured from the ground to the highest leaf tip. The plants were cut at the ground level and weighed. Then, the heads were cut open to measure the core length from the base. The number of leaves with tipburn, a physiological disorder, in each head was also recorded.

In general, the plant weight of the breeding lines was similar to or better than that of the commercial cultivars and resistant controls (Tables 13). The core length of the breeding lines was also similar to or shorter than that of the cultivars. A relatively short core length is generally preferred by most lettuce processors. The breeding lines had a similar or fewer number of leaves with tipburn compared with that of the cultivars. The red leaf lettuce breeding line USDA-07838 showed no tipburn during the trials conducted, whereas some commercial cultivars exhibited varying degrees of tipburn (Table 1). The romaine lettuce breeding lines USDA-14489 and USDA-17536 were similar to or taller than commercial cultivars (Table 3).

During these limited trials, the breeding lines performed well in the Salinas Valley, which is the major lettuce-producing region in the United States. They produced a high percentage of heads of adequate size, shape, and uniformity. The adaptation of the breeding lines to other lettuce-growing areas has not been evaluated.

Seed Availability

Limited seed samples are available from the corresponding author for distribution to all interested parties for research purposes, including the development and commercialization of new cultivars. Samples will also be deposited in the National Plant Germplasm System. It is requested that appropriate recognition be made if the breeding lines contribute to research or the development of new germplasm, breeding lines, or cultivars.

References Cited

  • Alvarez, J, Datnoff, LE & Nagata, RT. 1992 Crop rotation minimizes losses from corky root in Florida lettuce HortScience. 27 1 66 68 https://doi.org/10.21273/HORTSCI.27.1.66

    • Search Google Scholar
    • Export Citation
  • Brown, PR & Michelmore, RW. 1988 The genetics of corky root resistance in lettuce Phytopathology. 78 1145 1150

  • Grube, RC & Ochoa, OE. 2005 Comparative genetic analysis of field resistance to downy mildew in the lettuce cultivars ‘Grand Rapids’ and ‘Iceberg’ Euphytica. 142 205 215

    • Search Google Scholar
    • Export Citation
  • Keil, CB & Parrella, MP. 1990 Characterization of insecticide resistance in two colonies of Liriomyza trifolii (Diptera: Agromyzidae) J Econ Entomol. 83 18 26

    • Search Google Scholar
    • Export Citation
  • Lebeda, A & Zinkernagel, V. 2003 Evolution and distribution of virulence in the German population of Bremia lactucae Plant Pathol. 52 41 51

  • LeStrange, M, Koike, S, Valencia, J & Chaney, W. 1999 Spinach production in California Publ. 7212 3 4 University of California, Division of Agriculture and Natural Resources

    • Search Google Scholar
    • Export Citation
  • Mason, GA, Johnson, MW & Tabashnik, BE. 1987 Susceptibility of Liriomyza sativae and Liriomyza trifolii (Diptera:Agromyzidae) to permethrin and fenvalerate J Econ Entomol. 80 1262 1266

    • Search Google Scholar
    • Export Citation
  • Mou, B & Liu, YB. 2003 Leafminer resistance in lettuce HortScience. 38 4 570 572 https://doi.org/10.21273/HORTSCI.38.4.570

  • Mou, B & Liu, YB. 2004 Host plant resistance to leafminers in lettuce J Am Soc Hortic Sci. 129 3 383 388 https://doi.org/10.21273/JASHS.129.3.0383

    • Search Google Scholar
    • Export Citation
  • O’Brien, RD & van Bruggen, AHC. 1990 Soil fumigation with dazomet and methyl bromide for control of corky root of iceberg lettuce Plant Dis. 74 1022 1025

    • Search Google Scholar
    • Export Citation
  • Parrella, MP. 1987 Biology of Liriomyza Annu Rev Entomol. 32 201 224

  • Parrella, MP & Trumble, JT. 1989 Decline of resistance in Liriomyza trifolii (Diptera: Agromyzidae) in the absence of insecticide selection pressure J Econ Entomol. 82 365 368

    • Search Google Scholar
    • Export Citation
  • Patterson, CL, Grogan, RG & Campbell, RN. 1986 Economically important diseases of lettuce Plant Dis. 70 982 987

  • Ryder, EJ & Waycott, W. 1994 Crisphead lettuce resistant to corky root: Cultivars Glacier and Misty Day and 16 resistant breeding lines HortScience. 29 4 335 336 https://doi.org/10.21273/HORTSCI.29.4.335

    • Search Google Scholar
    • Export Citation
  • Ryder, EJ & Waycott, W. 1998 Crisphead lettuce resistant to tipburn: Cultivar Tiber and eight breeding lines HortScience. 33 5 903 904 https://doi.org/10.21273/HORTSCI.33.5.903

    • Search Google Scholar
    • Export Citation
  • Scheffer, SJ, Wijesekara, A, Visser, D & Hallett, RH. 2001 Polymerase chain reaction-restriction fragment-length polymorphism method to distinguish Liriomyza huidobrensis from L. langei (Diptera: Agromyzidae) applied to three recent leafminer invasions J Econ Entomol. 94 1177 1182

    • Search Google Scholar
    • Export Citation
  • Simko, I, Atallah, AJ, Ochoa, OE, Antonise, R, Galeano, CH, Truco, MJ & Michelmore, RW. 2013 Identification of QTLs conferring resistance to downy mildew in legacy cultivars of lettuce Sci Rep. 3 2875

    • Search Google Scholar
    • Export Citation
  • Subbarao, KV, Hubbard, JC & Schulbach, KF. 1997 Comparison of lettuce diseases and yield under subsurface drip and furrow irrigation Phytopathology. 87 877 883

    • Search Google Scholar
    • Export Citation
  • University of California 1992 Integrated pest management for cole crops and lettuce. Statewide Integrated Pest Management Project, Div. of Agr. and Natural Resources Publ. 3307 31 32

    • Search Google Scholar
    • Export Citation
  • van Bruggen, AHC. 1997 Corky root 28 29 Davis, RM, Subbarao, KV, Raid, RN & Kurtz, EA Compendium of lettuce diseases. APS Press St. Paul, MN

  • van Bruggen, AHC & Brown, PR. 1990 Distinction between infectious and noninfectious corky root of lettuce in relation to nitrogen fertilizer J Am Soc Hortic Sci. 115 762 770 https://doi.org/10.21273/JASHS.115.5.762

    • Search Google Scholar
    • Export Citation
  • van Bruggen, AHC, Brown, PR, Shennan, C & Greathead, AS. 1990 The effect of cover crops and fertilization with ammonium nitrate on corky root of lettuce Plant Dis. 74 584 589

    • Search Google Scholar
    • Export Citation
  • van Bruggen, AHC & Rubatzky, VE. 1992 Use of transplants instead of direct seeding to reduce corky root severity and losses due to corky root in iceberg lettuce Plant Dis. 76 703 708

    • Search Google Scholar
    • Export Citation
  • Yabuuchi, E, Kosako, Y, Naka, T, Suzuki, S & Yano, I. 1999 Proposal of Sphingomonas suberifaciens (van Bruggen, Jochimsen, and Brown 1990) comb. Nov., Sphingomonas natatoria (Sly 1985) cob. Nov., Sphingomonas ursincola (Yurkov et al. 1997) comb. Nov., and emendation of the genus Sphingomonas Microbiol Immunol. 43 339 349

    • Search Google Scholar
    • Export Citation
  • Fig. 1.

    Pedigrees of lettuce breeding lines USDA-07838, USDA-09456, USDA-09512, USDA-14489, and USDA-17536.

  • Fig. 2.

    Lettuce breeding lines in the field: (A, upper left): USDA-07838 (red leaf); (B, upper right): USDA-09456 (green leaf); (C, middle left): USDA-09512 (green leaf); (D, middle right): USDA-14489 (romaine); and (E, lower left): USDA-17536 (romaine).

  • Alvarez, J, Datnoff, LE & Nagata, RT. 1992 Crop rotation minimizes losses from corky root in Florida lettuce HortScience. 27 1 66 68 https://doi.org/10.21273/HORTSCI.27.1.66

    • Search Google Scholar
    • Export Citation
  • Brown, PR & Michelmore, RW. 1988 The genetics of corky root resistance in lettuce Phytopathology. 78 1145 1150

  • Grube, RC & Ochoa, OE. 2005 Comparative genetic analysis of field resistance to downy mildew in the lettuce cultivars ‘Grand Rapids’ and ‘Iceberg’ Euphytica. 142 205 215

    • Search Google Scholar
    • Export Citation
  • Keil, CB & Parrella, MP. 1990 Characterization of insecticide resistance in two colonies of Liriomyza trifolii (Diptera: Agromyzidae) J Econ Entomol. 83 18 26

    • Search Google Scholar
    • Export Citation
  • Lebeda, A & Zinkernagel, V. 2003 Evolution and distribution of virulence in the German population of Bremia lactucae Plant Pathol. 52 41 51

  • LeStrange, M, Koike, S, Valencia, J & Chaney, W. 1999 Spinach production in California Publ. 7212 3 4 University of California, Division of Agriculture and Natural Resources

    • Search Google Scholar
    • Export Citation
  • Mason, GA, Johnson, MW & Tabashnik, BE. 1987 Susceptibility of Liriomyza sativae and Liriomyza trifolii (Diptera:Agromyzidae) to permethrin and fenvalerate J Econ Entomol. 80 1262 1266

    • Search Google Scholar
    • Export Citation
  • Mou, B & Liu, YB. 2003 Leafminer resistance in lettuce HortScience. 38 4 570 572 https://doi.org/10.21273/HORTSCI.38.4.570

  • Mou, B & Liu, YB. 2004 Host plant resistance to leafminers in lettuce J Am Soc Hortic Sci. 129 3 383 388 https://doi.org/10.21273/JASHS.129.3.0383

    • Search Google Scholar
    • Export Citation
  • O’Brien, RD & van Bruggen, AHC. 1990 Soil fumigation with dazomet and methyl bromide for control of corky root of iceberg lettuce Plant Dis. 74 1022 1025

    • Search Google Scholar
    • Export Citation
  • Parrella, MP. 1987 Biology of Liriomyza Annu Rev Entomol. 32 201 224

  • Parrella, MP & Trumble, JT. 1989 Decline of resistance in Liriomyza trifolii (Diptera: Agromyzidae) in the absence of insecticide selection pressure J Econ Entomol. 82 365 368

    • Search Google Scholar
    • Export Citation
  • Patterson, CL, Grogan, RG & Campbell, RN. 1986 Economically important diseases of lettuce Plant Dis. 70 982 987

  • Ryder, EJ & Waycott, W. 1994 Crisphead lettuce resistant to corky root: Cultivars Glacier and Misty Day and 16 resistant breeding lines HortScience. 29 4 335 336 https://doi.org/10.21273/HORTSCI.29.4.335

    • Search Google Scholar
    • Export Citation
  • Ryder, EJ & Waycott, W. 1998 Crisphead lettuce resistant to tipburn: Cultivar Tiber and eight breeding lines HortScience. 33 5 903 904 https://doi.org/10.21273/HORTSCI.33.5.903

    • Search Google Scholar
    • Export Citation
  • Scheffer, SJ, Wijesekara, A, Visser, D & Hallett, RH. 2001 Polymerase chain reaction-restriction fragment-length polymorphism method to distinguish Liriomyza huidobrensis from L. langei (Diptera: Agromyzidae) applied to three recent leafminer invasions J Econ Entomol. 94 1177 1182

    • Search Google Scholar
    • Export Citation
  • Simko, I, Atallah, AJ, Ochoa, OE, Antonise, R, Galeano, CH, Truco, MJ & Michelmore, RW. 2013 Identification of QTLs conferring resistance to downy mildew in legacy cultivars of lettuce Sci Rep. 3 2875

    • Search Google Scholar
    • Export Citation
  • Subbarao, KV, Hubbard, JC & Schulbach, KF. 1997 Comparison of lettuce diseases and yield under subsurface drip and furrow irrigation Phytopathology. 87 877 883

    • Search Google Scholar
    • Export Citation
  • University of California 1992 Integrated pest management for cole crops and lettuce. Statewide Integrated Pest Management Project, Div. of Agr. and Natural Resources Publ. 3307 31 32

    • Search Google Scholar
    • Export Citation
  • van Bruggen, AHC. 1997 Corky root 28 29 Davis, RM, Subbarao, KV, Raid, RN & Kurtz, EA Compendium of lettuce diseases. APS Press St. Paul, MN

  • van Bruggen, AHC & Brown, PR. 1990 Distinction between infectious and noninfectious corky root of lettuce in relation to nitrogen fertilizer J Am Soc Hortic Sci. 115 762 770 https://doi.org/10.21273/JASHS.115.5.762

    • Search Google Scholar
    • Export Citation
  • van Bruggen, AHC, Brown, PR, Shennan, C & Greathead, AS. 1990 The effect of cover crops and fertilization with ammonium nitrate on corky root of lettuce Plant Dis. 74 584 589

    • Search Google Scholar
    • Export Citation
  • van Bruggen, AHC & Rubatzky, VE. 1992 Use of transplants instead of direct seeding to reduce corky root severity and losses due to corky root in iceberg lettuce Plant Dis. 76 703 708

    • Search Google Scholar
    • Export Citation
  • Yabuuchi, E, Kosako, Y, Naka, T, Suzuki, S & Yano, I. 1999 Proposal of Sphingomonas suberifaciens (van Bruggen, Jochimsen, and Brown 1990) comb. Nov., Sphingomonas natatoria (Sly 1985) cob. Nov., Sphingomonas ursincola (Yurkov et al. 1997) comb. Nov., and emendation of the genus Sphingomonas Microbiol Immunol. 43 339 349

    • Search Google Scholar
    • Export Citation
Beiquan Mou US Department of Agriculture, Agricultural Research Service, 1636 East Alisal Street, Salinas, CA 93905, USA

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Contributor Notes

I thank JoAnn Tanaka, Elisabeth Wood, Emi Kuroiwa, Alison Willis, David Milligan, and Sharon Benzen for technical assistance.

This research was supported in part by grants from the California Leafy Greens Research Program. The mentioning of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture.

B.M. is the corresponding author. E-mail: beiquan.mou@usda.gov.

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